Michael R. McGowen

Divergence date estimation and a comprehensive molecular tree of extant cetaceans.

Cetaceans are remarkable among mammals for their numerous adaptations to an entirely aquatic existence, yet many aspects of their phylogeny remain unresolved. Here we merged 37 new sequences from the nuclear genes RAG1 and PRM1 with most published molecular data for the group (45 nuclear loci, transposons, mitochondrial genomes), and generated a supermatrix consisting of 42,335 characters. The great majority of these data have never been combined. Model-based analyses of the supermatrix produced a solid, consistent phylogenetic hypothesis for 87 cetacean species. Bayesian analyses corroborated odontocete (toothed whale) monophyly, stabilized basal odontocete relationships, and completely resolved branching events within Mysticeti (baleen whales) as well as the problematic speciose clade Delphinidae (oceanic dolphins). Only limited conflicts relative to maximum likelihood results were recorded, and discrepancies found in parsimony trees were very weakly supported. We utilized the Bayesian supermatrix tree to estimate divergence dates among lineages using relaxed-clock methods. Divergence estimates revealed rapid branching of basal odontocete lineages near the Eocene-Oligocene boundary, the antiquity of river dolphin lineages, a Late Miocene radiation of balaenopteroid mysticetes, and a recent rapid radiation of Delphinidae beginning approximately 10 million years ago. Our comprehensive, time-calibrated tree provides a powerful evolutionary tool for broad-scale comparative studies of Cetacea.

Morphological and Molecular Evidence for a Stepwise Evolutionary Transition from Teeth to Baleen in Mysticete Whales

The origin of baleen in mysticete whales represents a major transition in the phylogenetic history of Cetacea. This key specialization, a keratinous sieve that enables filter-feeding, permitted exploitation of a new ecological niche and heralded the evolution of modern baleen-bearing whales, the largest animals on Earth. To date, all formally described mysticete fossils conform to two types: toothed species from Oligocene-age rocks ( approximately 24 to 34 million years old) and toothless species that presumably utilized baleen to feed (Recent to approximately 30 million years old). Here, we show that several Oligocene toothed mysticetes have nutrient foramina and associated sulci on the lateral portions of their palates, homologous structures in extant mysticetes house vessels that nourish baleen. The simultaneous occurrence of teeth and nutrient foramina implies that both teeth and baleen were present in these early mysticetes. Phylogenetic analyses of a supermatrix that includes extinct taxa and new data for 11 nuclear genes consistently resolve relationships at the base of Mysticeti. The combined data set of 27,340 characters supports a stepwise transition from a toothed ancestor, to a mosaic intermediate with both teeth and baleen, to modern baleen whales that lack an adult dentition but retain developmental and genetic evidence of their ancestral toothed heritage. Comparative sequence data for ENAM (enamelin) and AMBN (ameloblastin) indicate that enamel-specific loci are present in Mysticeti but have degraded to pseudogenes in this group. The dramatic transformation in mysticete feeding anatomy documents an apparently rare, stepwise mode of evolution in which a composite phenotype bridged the gap between primitive and derived morphologies; a combination of fossil and molecular evidence provides a multifaceted record of this macroevolutionary pattern.

A phylogenetic blueprint for a modern whale

The emergence of Cetacea in the Paleogene represents one of the most profound macroevolutionary transitions within Mammalia. The move from a terrestrial habitat to a committed aquatic lifestyle engendered wholesale changes in anatomy, physiology, and behavior. The results of this remarkable transformation are extant whales that include the largest, biggest brained, fastest swimming, loudest, deepest diving mammals, some of which can detect prey with a sophisticated echolocation system (Odontoceti - toothed whales), and others that batch feed using racks of baleen (Mysticeti - baleen whales). A broad-scale reconstruction of the evolutionary remodeling that culminated in extant cetaceans has not yet been based on integration of genomic and paleontological information. Here, we first place Cetacea relative to extant mammalian diversity, and assess the distribution of support among molecular datasets for relationships within Artiodactyla (even-toed ungulates, including Cetacea). We then merge trees derived from three large concatenations of molecular and fossil data to yield a composite hypothesis that encompasses many critical events in the evolutionary history of Cetacea. By combining diverse evidence, we infer a phylogenetic blueprint that outlines the stepwise evolutionary development of modern whales. This hypothesis represents a starting point for more detailed, comprehensive phylogenetic reconstructions in the future, and also highlights the synergistic interaction between modern (genomic) and traditional (morphological+paleontological) approaches that ultimately must be exploited to provide a rich understanding of evolutionary history across the entire tree of Life.

Timing and Tempo of Early and Successive Adaptive Radiations in Macaronesia

The flora of Macaronesia, which encompasses five Atlantic archipelagos (Azores, Canaries, Madeira, Cape Verde, and Salvage), is exceptionally rich and diverse. Spectacular radiation of numerous endemic plant groups has made the Macaronesian islands an outstanding area for studies of evolution and speciation. Despite intensive investigation in the last 15 years, absolute age and rate of diversification are poorly known for the flora of Macaronesia. Here we report molecular divergence estimates and rates of diversification for five representative, putative rapid radiations of monophyletic endemic plant lineages across the core eudicot clade of flowering plants. Three discrete windows of colonization during the Miocene and early Pliocene are suggested for these lineages, all of which are inferred to have had a single colonization event followed by rapid radiation. Subsequent inter-archipelago dispersal events into Madeira and the Cape Verdes took place very recently during the late Pliocene and Pleistocene after initial diversification on the Canary Islands. The tempo of adaptive radiations differs among the groups, but is relatively rapid compared to continental and other island radiations. Our results demonstrate that opportunity for island colonization and successful radiation may have been constrained to discrete time periods of profound climatic and geological changes in northern African and the Mediterranean.

Comparative analysis of encephalization in mammals reveals relaxed constraints on anthropoid primate and cetacean brain scaling

There is a well‐established allometric relationship between brain and body mass in mammals. Deviation of relatively increased brain size from this pattern appears to coincide with enhanced cognitive abilities. To examine whether there is a phylogenetic structure to such episodes of changes in encephalization across mammals, we used phylogenetic techniques to analyse brain mass, body mass and encephalization quotient (EQ) among 630 extant mammalian species. Among all mammals, anthropoid primates and odontocete cetaceans have significantly greater variance in EQ, suggesting that evolutionary constraints that result in a strict correlation between brain and body mass have independently become relaxed. Moreover, ancestral state reconstructions of absolute brain mass, body mass and EQ revealed patterns of increase and decrease in EQ within anthropoid primates and cetaceans. We propose both neutral drift and selective factors may have played a role in the evolution of brain–body allometry.

Genome-wide adaptive complexes to underground stresses in blind mole rats Spalax

The blind mole rat (BMR), Spalax galili, is an excellent model for studying mammalian adaptation to life underground and medical applications. The BMR spends its entire life underground, protecting itself from predators and climatic fluctuations while challenging it with multiple stressors such as darkness, hypoxia, hypercapnia, energetics and high pathonecity. Here we sequence and analyse the BMR genome and transcriptome, highlighting the possible genomic adaptive responses to the underground stressors. Our results show high rates of RNA/DNA editing, reduced chromosome rearrangements, an over-representation of short interspersed elements (SINEs) probably linked to hypoxia tolerance, degeneration of vision and progression of photoperiodic perception, tolerance to hypercapnia and hypoxia and resistance to cancer. The remarkable traits of the BMR, together with its genomic and transcriptomic information, enhance our understanding of adaptation to extreme environments and will enable the utilization of BMR models for biomedical research in the fight against cancer, stroke and cardiovascular diseases.

The vestigial olfactory receptor subgenome of odontocete whales: phylogenetic congruence between gene-tree reconciliation and supermatrix methods.

The macroevolutionary transition of whales (cetaceans) from a terrestrial quadruped to an obligate aquatic form involved major changes in sensory abilities. Compared to terrestrial mammals, the olfactory system of baleen whales is dramatically reduced, and in toothed whales is completely absent. We sampled the olfactory receptor (OR) subgenomes of eight cetacean species from four families. A multigene tree of 115 newly characterized OR sequences from these eight species and published data for Bos taurus revealed a diverse array of class II OR paralogues in Cetacea. Evolution of the OR gene superfamily in toothed whales (Odontoceti) featured a multitude of independent pseudogenization events, supporting anatomical evidence that odontocetes have lost their olfactory sense. We explored the phylogenetic utility of OR pseudogenes in Cetacea, concentrating on delphinids (oceanic dolphins), the product of a rapid evolutionary radiation that has been difficult to resolve in previous studies of mitochondrial DNA sequences. Phylogenetic analyses of OR pseudogenes using both gene-tree reconciliation and supermatrix methods yielded fully resolved, consistently supported relationships among members of four delphinid subfamilies. Alternative minimizations of gene duplications, gene duplications plus gene losses, deep coalescence events, and nucleotide substitutions plus indels returned highly congruent phylogenetic hypotheses. Novel DNA sequence data for six single-copy nuclear loci and three mitochondrial genes (> 5000 aligned nucleotides) provided an independent test of the OR trees. Nucleotide substitutions and indels in OR pseudogenes showed a very low degree of homoplasy in comparison to mitochondrial DNA and, on average, provided more variation than single-copy nuclear DNA. Our results suggest that phylogenetic analysis of the large OR superfamily will be effective for resolving relationships within Cetacea whether supermatrix or gene-tree reconciliation procedures are used.

Dolphin genome provides evidence for adaptive evolution of nervous system genes and a molecular rate slowdown

Cetaceans (dolphins and whales) have undergone a radical transformation from the original mammalian bodyplan. In addition, some cetaceans have evolved large brains and complex cognitive capacities. We compared approximately 10 000 protein-coding genes culled from the bottlenose dolphin genome with nine other genomes to reveal molecular correlates of the remarkable phenotypic features of these aquatic mammals. Evolutionary analyses demonstrated that the overall synonymous substitution rate in dolphins has slowed compared with other studied mammals, and is within the range of primates and elephants. We also discovered 228 genes potentially under positive selection (dN/dS > 1) in the dolphin lineage. Twenty-seven of these genes are associated with the nervous system, including those related to human intellectual disabilities, synaptic plasticity and sleep. In addition, genes expressed in the mitochondrion have a significantly higher mean dN/dS ratio in the dolphin lineage than others examined, indicating evolution in energy metabolism. We encountered selection in other genes potentially related to cetacean adaptations such as glucose and lipid metabolism, dermal and lung development, and the cardiovascular system. This study underlines the parallel molecular trajectory of cetaceans with other mammalian groups possessing large brains.

Toward the resolution of an explosive radiation—A multilocus phylogeny of oceanic dolphins (Delphinidae)

Oceanic dolphins (Delphinidae) are the product of a rapid radiation that yielded ∼36 extant species of small to medium-sized cetaceans that first emerged in the Late Miocene. Although they are a charismatic group of organisms that have become poster children for marine conservation, many phylogenetic relationships within Delphinidae remain elusive due to the slow molecular evolution of the group and the difficulty of resolving short branches from successive cladogenic events. Here I combine existing and newly generated sequences from four mitochondrial (mt) genes and 20 nuclear (nu) genes to reconstruct a well-supported phylogenetic hypothesis for Delphinidae. This study compares maximum-likelihood and Bayesian inference methods of several data sets including mtDNA, combined nuDNA, gene trees of individual nuDNA loci, and concatenated mtDNA+nuDNA. In addition, I contrast these standard phylogenetic analyses with the species tree reconstruction method of Bayesian concordance analysis (BCA). Despite finding discordance between mtDNA and individual nuDNA loci, the concatenated matrix recovers a completely resolved and robustly supported phylogeny that is also broadly congruent with BCA trees. This study strongly supports groupings such as Delphininae, Lissodelphininae, Globicephalinae, Sotalia+Delphininae, Steno+Orcaella+Globicephalinae, and Leucopleurus acutus, Lagenorhynchus albirostris, and Orcinus orca as basal delphinid taxa.

Molecular evolution tracks macroevolutionary transitions in Cetacea

Cetacea (whales, dolphins, and porpoises) is a model group for investigating the molecular signature of macroevolutionary transitions. Recent research has begun to reveal the molecular underpinnings of the remarkable anatomical and behavioral transformation in this clade. This shift from terrestrial to aquatic environments is arguably the best-understood major morphological transition in vertebrate evolution. The ancestral body plan and physiology were extensively modified and, in many cases, these crucial changes are recorded in cetacean genomes. Recent studies have highlighted cetaceans as central to understanding adaptive molecular convergence and pseudogene formation. Here, we review current research in cetacean molecular evolution and the potential of Cetacea as a model for the study of other macroevolutionary transitions from a genomic perspective.